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Hybridizing Old and New World camelids: Camelus dromedarius x Lama guanicoe

  • Camel Reproduction Centre
  • Camel Reproduction Centre Dubai UAE

Abstract and Figures

Thirty female dromedary camels were inseminated on a total of 50 occasions with 2-4 ml of fresh guanaco semen diluted with an equal volume of commercially available camel semen extender. Similarly, nine female guanacos were inseminated on 34 occasions with 4-6 ml of fresh, diluted camel semen. Only two of the dromedary females conceived; one aborted a female foetus on day 260 of gestation and the other gave birth to a stillborn female calf on day 365. Six conceptions occurred in the female guanacos. Two of these conceptuses, diagnosed by ultrasound, were resorbed between days 25 and 40 of gestation, one female foetus was aborted on day 291, another female foetus was aborted on day 302, and one female calf was stillborn on day 365 of gestation. The sixth foetus, a male, was born prematurely but alive after a 328-day gestation. It had a phenotypic appearance intermediate between that of a camel and a guanaco and its hybrid parentage was confirmed by the DNA fingerprinting of eight llama microsatellites. To our knowledge, this is the first viable hybrid ever to be produced between Old World and New World camelids, which have been reproductively isolated from one another for at least 11 million years. The preponderance of female hybrids is in accordance with Haldane's law. Histological examination of their ovaries revealed a failure of meiosis, with only an occasional abnormal oocyte surrounded by follicle cells. Although the diploid chromosone number of camels and guanacos is the same (2n = 74), sufficient genetic change has taken place to make the pairing of homologous chromosomes no longer possible.
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Hybridizing Old and New World camelids:
Camelus dromedarius Lama guanicoe
J. A. Skidmore1, M. Billah1, M. Binns2, R. V. Short3and W. R. Allen4*
1The Camel Reproduction Centre, PO Box 11808, Dubai, United Arab Emirates
2Animal HealthTrust, Lanwades Park, Newmarket, Su¡olk CB8 7UU, UK
3The Royal Women's Hospital, Carlton, Victoria 3053, Australia
4Department of ClinicalVeterinary Medicine, Equine Fertility Unit, University of Cambridge, Mertoun Paddocks, Woodditton Road,
Newmarket, Su¡olk CB8 9BH, UK
Thirty female dromedary camels were inseminated on a total of 50 occasions with 2^4 ml of fresh
guanaco semen diluted with an equal volume of commercially available camel semen extender. Similarly,
nine female guanacos were inseminated on 34 occasions with 4^6 ml of fresh, diluted camel semen. Only
two of the dromedary females conceived; one aborted a female foetus on day 260 of gestation and the
other gave birth to a stillborn female calf on day 365. Six conceptions occurred in the female guanacos.
Two of these conceptuses, diagnosed by ultrasound, were resorbed between days 25 and 40 of gestation,
one female foetus was aborted on day 291, another female foetus was aborted on day 302, and one female
calf was stillborn on day 365 of gestation. The sixth foetus, a male, was born prematurely but alive after
a 328-day gestation. It had a phenotypic appearance intermediate between that of a camel and a
guanaco and its hybrid parentage was con¢rmed by the DNA ¢ngerprinting of eight llama microsatel-
lites. To our knowledge, this is the ¢rst viable hybrid ever to be produced between Old World and New
World camelids, which have been reproductively isolated from one another for at least 11 million years.
The preponderance of female hybrids is in accordance with Haldane's law. Histological examination of
their ovaries revealed a failure of meiosis, with only an occasional abnormal oocyte surrounded by follicle
cells. Although the diploid chromosone number of camels and guanacos is the same (2n74), su¤cient
genetic change has taken place to make the pairing of homologous chromosomes no longer possible.
Keywords: camel; guanaco; hybrid
The family Camelidae is of great antiquity. Palaeontolo-
gical evidence suggests they split o¡ from the other
cloven-hoofed mammals in the Eocene ca. 40^45 million
years (Myr) ago (Romer 1966; Simpson 1980), and split
again into the genera Camelus and Lama in North
America relatively soon after, ca. 30 Myr ago (Webb 1974;
Harrison 1979). However, more recent molecular studies
of mitochondrial DNA (mtDNA) mutation rates suggest
that the split may have occurred ca. 11Myr ago (Stanley
et al. 1994). Today, there remains two species of large, Old
World camels indigenous to Asia and Africa, namely, the
two-humped Bactrian (Camelus bactrianus) and the one-
humped dromedary (Camelus dromedarius), and four species
of smaller New World camels in South America, the
domesticated llama (Lama glama), its probable wild ante-
cedent the guanaco (Lama guanicoe), the domesticated
alpaca (Lama pacos) and its possible wild ancestor the
vicu·a (Lama vicugna). During one of the early ice ages,
the cameloids crossed the land bridge created between
North America and Asia in the region of the Bering
Straits and then radiated through Asia into Eastern
Europe and the Middle East. They were unknown to the
ancient Egyptians (Zeuner 1963), and may have been
introduced into North Africa by man. The lamoids
migrated southwards and crossed the land bridge into
South America. All Camelidae had become extinct in
North America before historic times.
Today, the New and Old World camelids show some
remarkable anatomical and physiological similarities, and
some equally striking contrasts as a result of their adapta-
tion to di¡erent environmental extremes. For example,
they all share the same diploid chromosome number
(2n74; Hsu & Benirschke 1969), they are all induced
ovulators (San-Martin et al. 1968; Musa & Abusineima
1978; El Wishy 1987) and they all have a bicornuate
uterus in which the left horn is considerably larger than
the right and always acts as the site of implantationö
although ovulation occurs equally frequently from the left
and right ovaries (Arthur et al. 1985; El Wishy 1988). They
also share the same di¡use, non-invasive epitheleochorial
placenta (Van Lennep 1963; Steven et al. 1980; Skidmore
et al. 1996a). They di¡er in that the New World camelids
are small, cloven-hoofed, and have a dense, ¢ne-wool
coat that enables them to survive in the extremely low
temperatures of the snowy deserts of the high Andes,
whereas the Old World camelids are much larger, have a
single broad footpad and a less dense hairy coat, and are
adapted to the extreme diurnal temperature variations
Proc. R. Soc. Lond. B (1999) 26 6, 649^656 649 &1999 The Royal Society
Received 2 December 1998 Accepted 21 December 1998
*Author for correspondence.
and scarce food supplies in the mountainous deserts of
Mongolia and the low-lying deserts of Arabia. Both the
Old World camelids will hybridize with one another to
produce fertile o¡spring, and all the New World species
will similarly hybridize with each other and produce
fertile young (Gray 1972). However, to our knowledge
there are no published accounts of induced hybridization
between Old and New World camelids, which could not
occur naturally due to geographical separation and great
disparity in body size. The object of the present study was
to attempt to hybridize dromedaries with guanacos, using
arti¢cial insemination.
Thirty adult female dromedary camels aged 6^14 years and
estimated to weigh between 380 kg and 450 kg, and two adult
male dromedaries aged ¢ve and eight years and estimated to
weigh 550^6 00 kg that had been trained to ejaculate into a
modi¢ed bull arti¢cial vagina (AV), were maintained as part of
the experimental herd at the Camel Reproduction Centre in
Dubai, UAE. Nine females (estimated age, 3^7 years; estimated
weights, 75^80 kg) and one young male (estimated age, 3^4
years; estimated weight, 85kg) guanacos were captured from a
nearby wildlife park, translocated to pens at the Camel Repro-
duction Centre and partly tamed.
During the camel breeding season in the Arabian Gulf region
(November ^April) of 1995^1996 and 1996^1997, the ovarian
follicular wave patterns of the dromedaries were monitored by
serial trans-rectal ultrasound examinations, as described by
Skidmore et al. (1995). When a dominant follicle reached a
diameter of 1.3^1.6 cm the camel was given an intravenous injec-
tion of 20 mg of the GnRH analogue, buserelin (Receptal;
Hoechst Animal Health, Bedfordshire, UK). The camel was
then inseminated with the whole ejaculate from a male guanaco
(2^4 ml of semen; 15^4 0107spermatozoa; 50^70% motility)
collected with the AV and diluted with an equal volume of a
commercial semen extender designed for camel semen (Green
Bu¡er; IMV Ltd, L 'Aigle, France) containing 10% v/v egg
yolk. This was deposited in the body of the uterus using a plastic
bovine insemination catheter guided manually through the
cervix by the operator's sterile gloved hand in the vagina. These
inseminations were given either once, 24 h after treatment with
GnRH (n45), or twice, at the time of GnRH therapy and
again 24 h later (n5).
The female guanacos were also monitored by trans-rectal
ultrasonography and when the dominant follicle attained a
diameter of 0.8^0.9 cm, each guanaco was given an intra-
muscular ( IM) injection of 10 mg buserelin and inseminated
either once 24 h later (n22) or t wice 24 h apart (n11) with a
4^6 ml aliquot of camel semen diluted 1:1 with Green Bu¡er
containing 10% v/v egg yolk. The inseminate was prepared
from a camel ejaculate (3^8 ml; 50^150107spermatozoa; 60^
80% motility) and it was also deposited in the uterine body by
means of a manually guided insemination catheter passed
through the cervix.
Ovulation in the camels and guanacos was diagnosed by
ultrasound examination of the ovaries 48 h after the GnRH
injection (Skidmore et al. 1995) and con¢rmed subsequently by
measuring a rise in progesterone concentrations in peripheral
serum samples recovered daily from each animal from the time
of the GnRH treatment. A chemiluminescent progesterone
assay developed for human serum (Amerlite; Kodak Diagnostics
Ltd, Buckinghamshire, UK) and validated for camel serum by
Skidmore et al. (1996b) was used. Pregnancy was suspected
when serum progesterone concentrations remained elevated
beyond 12 d after insemination, and was subsequently con¢rmed
by ultrasound examination of the uterus. A discrete accumula-
tion of conceptus £uid in the lumen of the left uterine horn was
¢rst observed between days 18 and 20, an echogenic embryo
suspended within the £uid could be distinguished between days
20 and 23, and a foetal heartbeat was identi¢able between days
25 and 27 (Skidmore et al. 1992).
In two of the inseminated camels it was suspected that luteal
function was impaired, as judged, using ultrasonography, by the
small size of the corpus luteum and low serum progesterone
concentrations. These animals were, therefore, given daily IM
injections of 6 ml of a 25 mg ml71suspension of progesterone in
peanut oil (Intervet Laboratories, Cambridge, UK) from the
sixth day after insemination until one of them was con¢rmed as
non-pregnant by ultrasound examination on days 22 and 25 and
the other aborted a dead and partly autolysed foetus on day 260
of gestation.
Thirty dromedary females were inseminated on 50
occasions with diluted guanaco semen 24 h after an injec-
tion of GnRH analogue was given to induce ovulation,
but only two conceived (table 1). One camel aborted a
dead and partly autolysed female foetus (GC2) on day
260 of gestation while still receiving progesterone therapy.
The other calved unattended and spontaneously on day
365 of gestation but the female calf was stillborn (GC1).
Post-mortem examination showed that the calf had devel-
oped normally but its lungs had not been aerated.
Six conceptions occurred in the nine female guanacos
that were inseminated with diluted camel semen after a
GnRH injection to induce ovulation on 34 occasions
(table 1). One conceptus failed to develop an embryo and
the vesicle shrank and disappeared ultrasonographically
between 22 and 30 days after insemination (CG3). In a
second guanaco, the foetal heartbeat ceased between the
two serial ultrasound examinations performed 30 and 39
days after insemination, and the remaining conceptus
£uid and membranes shrank and disappeared altogether
over the following 20 days (CG4). One female foetus was
aborted on day 291 (CG1), another female foetus was
aborted on day 302 (CG6) and one female foetus was
stillborn on day 365 of gestation (CG2). The sixth
guanaco calved spontaneously and unaided on day 328 of
gestation and produced a live male calf, Rama (CG5),
that was somewhat premature and weighed only 5.5 kg.
This was less than the weight of a newborn guanaco at
term (8^10 kg) and appreciably less than the weight of a
newborn camel calf ( 30 kg).
(a) Rearing the calf
The hybrid calf showed no tooth eruption at birth, an
indication of its prematurity, and since its mother had no
mammary development and showed no maternal beha-
viour, it was hand-reared on fresh camel milk obtained
daily from a dromedary that had calved 24 h earlier.
Initially, each feed of 30^50 ml of camel milk was o¡ered
at regular intervals, every 1.5 h throughout the day and
night. After 48 h, the feeding interval was extended to 2 h
650 J. A. Skidmore and others Hybrids between camels and guanacos
Proc. R. Soc. Lond. B (1999)
and the daily intake increased to 120 0 ml. This pattern
was continued for the ¢rst month but, during the second
and third months, the feeding interval was increased
gradually to 4 h. The volume of milk consumed per feed
increased from 300 ml at the end of the ¢rst month to
700 ml by the end of the fourth month, by which time the
feeding interval had extended to 8h. A compounded `calf
starter' feed and hay were o¡ered to the calf from
30 days of age and its daily intake of these solids had
increased to around 500 g by the fourth month. Initially,
the calf gained weight at a rate of 0.2 kg per day over the
¢rst seven days but thereafter the gain increased to
approximately 2.5 kg per week (¢gure 1).
At nine months of age the hybrid calf was in good
health. He exhibited the woolly ¢bre coat and the nose
and nostrils of the New World camelids, but his ears and
tail were midway in length between those of camels and
guanacos (¢gure 2c). Similarly, his feet were an inter-
mediate of the single two-toed conjoined footpad of
camels and the cloven hooves of guanacos (¢gures 2d^f).
However, unlike guanacos, he showed no skin glands on
the lateral or medial aspects of the tarsus and there was
no sign of the hump that would be present on a camel calf
of the same age. He had two small testicles, measuring
4 cm 2cm and palpable in the scrotum ca. 4 cm below
the anus.
Hybrids between camels and guanacos J. A. Skidmore and others 651
Proc. R. Soc. Lond. B (1999)
Table 1. Hybrid pregnancies
(C represents camel; G represents guanaco.)
number sire dam
date of
foetal weight
(kg) sex
duration of
gestation (days)
camel guanaco
CG1 Musehan 3 3/11/96 2.5 female 291 (aborted)
CG2 Musehan 3 4/1/98 9.0 female 365 (stillborn)
CG3 Young One or Musehan 1 ööö30 (resorbed)
CG4 Young One or Musehan 4 ööö40 (resorbed)
CG5 Musehan or Young One 1 14/1/98 5.5 male 328 (born live)
CG6 Musehan 6 3/11/98 3.7 female 302 (aborted)
guanaco camel
GC1 Whalid 660 18/2/97 30.0 female 365 (stillborn)
GC2 Whalid 1610 3/2/98 1.0 female 260 (aborted)
Figure 1. Growth curve for the male dromedary guanaco calf, Rama, during the ¢rst nine months. Open circles, height in
centimetres; closed circles, weight in kilograms.
652 J. A. Skidmore and others Hybrids between camels and guanacos
Proc. R. Soc. Lond. B (1999)
Figure 2. (a) The dromedary sire, Musehan, and the guanaco dam (no. 1) with their two-day old hybrid calf. (b,c) The hybrid
calf, Rama, at two days and two months of age, respectively. (d^f) Comparison of the front footpads of (d) an adult female
guanaco, (e) the dromedaryguanaco hybri d, and ( f) a newborn dromedary camel calf.
Hybrids between camels and guanacos J. A. Skidmore and others 653
Proc. R. Soc. Lond. B (1999)
Figure 3. Histological sections of the ovaries recovered from (a) a full-term guanaco calf and (b^d) three guanacodromedary
hybrid foetuses (see table 1). (a) The guanaco guanaco calf stillborn at full term. The cortex is packed with `normal'-looking
oocytes contained within primary, secondary or tertiary follicles. (b) Hybrid calf CG2, showing a compact, ¢brous cortex
containing many eosinophylic cords which may represent dead or dying oogonia in P£u
«ger's cords, unable to enter meiosis. No
oocytes or follicles are visible. (c) A high-power section of the cortical region of the ovary from hybrid GC1 showing heavily
eosinophylic oogonia arranged in clumps or cords, but no oocytes or follicle cells. (d) A high-power section of the ovary from
hybrid CG1 showing one unhealthy looking oocyte surrounded by degenerating follicle cells and an adjacent, even more
degenerative, oocyte with a pycnotic nucleus and barely recognizable follicle cells. Scale bars, 100 mm.
Behaviourally, Rama clearly showed features of his
hybrid genotype. His vocalization was an unusual highly
pitched `croak' uttered on expiration, which has discern-
ible elements of both parental species. He urinated
backwards in a series of spurts like both guanacos and
camels, but defecated while moving which is similar to
camels but not guanacos, which tend to defecate in one
place. He chewed cud by alternating from one side to the
other in a manner similar to guanacos. He developed
aggressive behaviour towards adult female guanacos,
which included laying his ears back, rearing onto his hind
legs, striking out with his front feet and attempting to
spit; none of these movements are exhibited by young
(b) Post-mortem ¢ndings
The ovaries of hybrid foetus GC2 were too decom-
posed to permit histological examination. Ovaries were
recovered from the hybrid foetus, CG1, aborted on day
291 of gestation; the two hybrid calves, CG2 and GC1,
stillborn on day 365; from a newborn full-term guanaco
calf; and from a dromedary foetus aborted at 12 months
of gestation. Pieces of ovarian tissue were ¢xed in 10%
phosphate-bu¡ered formaldehyde solution, embedded in
para¤n wax, sectioned at 5 mm thickness and stained
with haematoxylin and eosin (H & E).
Histologically, ovaries from the full-term guanaco
revealed a number of tertiary Graa¢an follicles with a
£uid-¢lled antrum, and many primordial and secondary
follicles throughout the outer cortex, with oocytes
surrounded by single or multiple layers of follicle cells
(¢gure 3a). The ovaries of the camel foetus contained
numerous large tertiary follicles, of up to 0.5 cm in
diameter, and many primordial and secondary follicles
throughout the outer ovarian cortex.
The ovaries of the three hybrids presented a very
di¡erent appearance. GC1, stillborn at 365 days, showed
heavily eosinophilic oogonia arranged in clumps or cords,
but there was no evidence that any of the oogonia had
entered meiosis as there were no signs of any oocytes with
their characteristic layer of surrounding follicle cells
(¢gure 3c). CG2, also stillborn at 365 days, showed a
compact, ¢brous ovarian cortex with many eosinophilic
cords which may represent dead or dying oogonia that
were unable to enter meiosis (¢gure 3b). There were
occasional degenerating oocytes with surrounding follicle
cells. The ovaries of CG1, aborted at 291 days, showed a
similar picture, with an occasional degenerate-looking
oocyte surrounded by degenerating follicle cells,
suggesting that a few oogonia had been able to initiate
meiosis. However, chromosomal pairing was probably
incomplete and resulted in the death of the oocyte and
follicle cells that it had induced to form around itself
(¢gure 3d).
(c) Parentage analysis
Blood samples were collected into preservative-free
sodium heparin tubes from the two male camels,
Musehan and Young One, that had supplied the semen
used for arti¢cial insemination; from guanaco no. 1, the
mother of the calf; and from Rama the calf (CG5, see
table 1). DNA was extracted from a 5 ml aliquot of whole
blood using a commercial kit (Nucleon; Scotlab Ltd,
Coatbridge, Scotland). Subsequently, genotypes for each
animal were obtained by performing PCR on the
extracted DNA, using eight llama microsatellites under
the PCR conditions described by Lang et al. (1996).
Fluorescent dUTP was incorporated into the PCR
products which were then electrophoresed on an ABI377
automated sequencer and the data analysed using
Genescan 2.1.
The results of the genotyping analysis using the llama
microsatellites are presented in table 2. They are fully
consistent with the hybrid being the o¡spring of the
female guanaco and the male camel, Musehan, with
exclusion of the second male camel, Young One, on the
basis of two of the markers,YWLL08 and YWLL44. The
size ranges for the alleles ampli¢ed from the guanaco
sample were all within the ranges published by Lang et al.
(1996), except those of markers YWLL19 and YWLL44.
The variation observed with YWLL44 was relatively
small, the observed alleles being 83/112, compared with
the published range of 86^120. However, for YWLL19,
the size of the observed allele (243) di¡ered signi¢cantly
from the published size range of 137^161.
To our knowledge, this is the ¢rst report of a viable
hybrid between Old and New World camelids. It was
achieved by using arti¢cial insemination and hormone
therapy to overcome the marked di¡erences between the
two parental species in terms of their body size and their
oestrous behaviour (England et al. 1971; Skidmore et al.
1996b). Considering the other marked anatomical,
physiological and behavioural di¡erences that have
evolved between the two separated groups to enable them
to survive in very harsh and diametrically opposed
enviroments, it is quite remarkable that their basic repro-
ductive mechanisms have been su¤ciently conserved to
permit hybridization. Although the diploid chromosome
number has remained unchanged at 2n74 for all
camelids, the failure of meiosis in the ovaries of all the
hybrids suggests that su¤cient genetic change must have
654 J. A. Skidmore and others Hybrids between camels and guanacos
Proc. R. Soc. Lond. B (1999)
Table 2. Genotyping results for the eight llama microsatellites tested on the camel guanaco hybrid and its parents
guanaco (no. 1) 135/143 243/243 215/217 153/155 186/186 133/133 83/112 107/111
hybrid (CG5) 135/158 243/243 205/215 133/155 172/186 133/133 83/103 107/107
Musehan 158/158 243/243 205/205 131/133 172/172 133/133 103/107 107/109
Young One 128/130 243/243 205/205 131/133 172/172 133/133 107/107 107/109
occurred during the millions of years of reproductive
isolation to disrupt the pairing of homologous chromo-
somes as they enter meiosis. It remains to be seen whether
the surviving male hybrid will be capable of producing
any sperm when he reaches puberty, although this seems
most unlikely.
The conception rates achieved when inseminating
dromedaries with semen from a single male guanaco (two
conceptions from the insemination of 30 fertile females on
50 separate occasions) and guanacos with semen from
two dromedary males of known fertility (six conceptions
from the insemination of nine animals on 34 occasions)
were much lower than the 50^55% conception rate
achieved routinely in the same laboratory when insemi-
nating dromedaries with dromedary semen. This might
indicate impaired fertilization and/or early embryonic
development. The conception rate appeared to be higher
in guanacos inseminated with dromedary semen than in
the dromedaries inseminated with guanaco semen, which
is reminiscent of the di¡erence in fertility between other
reciprocal interspeci¢c mammalian matings, such as
between rabbit and hare (Chang et al. 1964), sheep and
goat (Hancock et al. 1968), and horse and donkey (Allen
& Short 1997). It could be explained by di¡erences in
sperm^egg binding; camel spermatozoa might bind more
readily to guanaco oocytes than vice versa. The causes of
the late foetal deaths and stillbirths in the camelid
hybrids remain unexplained.
DNA genotyping was used to con¢rm that the hybrid
was the product of the mating between the female
guanaco and a male dromedary camel and it also deter-
mined the actual sire between the two possible conten-
ders. The combined exclusion probabilities of the eight
microsatellites used, based on their individual exclusion
probabilities in llamas and alpacas, is 0.9997. While the
corresponding exclusion probability in Old World came-
lids has not been determined, it would be surprising if
this panel of microsatellites did not display useful poly-
morphism in both the Bactrian and dromedary camels.
The allele size observed with the marker YWLL19 in all
four animals typed here (243 bp) di¡ers signi¢cantly
from the published allele size range in llamas and alpacas
(137^161bp). The primer sequences for YWLL19 were
veri¢ed as correct and no obvious explanation exists for
this discrepancy. It was of interest to ¢nd that the allele
sizes observed with the camel samples for ¢ve of the
markers (YWLL08, YWLL19, YWLL29, YWLL36 and
YWLL40) fell outside the ranges for these markers
observed in llamas and alpacas, thereby suggesting that
these microsatellites have diverged considerably in Old
and New World camelids since their split 11^30 Myr ago.
Perhaps one of the most interesting aspects of this study
relates to the gestation length and size at birth of the
surviving hybrid. The duration of gestation (328 days)
and birth weight (5.5 kg) are close to the normal range
for guanaco pregnancy, but are signi¢cantly less than the
395 days 30 kg of a normal dromedary pregnancy.
Thus, there appears to have been a complete maternal
override of the paternal genotype during pregnancy,
which is perhaps a result of the size constraint imposed
by a restricted area of the endometrium upon the di¡use,
non-invasive epitheliochorial placenta. Once born,
however, the hybrid calf had shown signi¢cant catch-up
growth and at nine months of age was 2.5 cm taller than
his mother. It will be interesting to see whether this
pronounced intra-uterine growth retardation has any
adverse e¡ects on his subsequent health and well-being,
as the Barker hypothesis (Barker 1995) would predict.
The apparent female skewing of the sex ratio in the
foetuses and neonate (one male:¢ve females) is in accor-
dance with Haldane's law, which states that `when in the
F1o¡spring of two di¡erent animal species one sex is
absent, rare or sterile, that sex is the heterozygous sex'
(Haldane 1922). The reason for this skewing may be that
the mutation rate of genes of the unpaired segment of the
Y chromosome is apparently much higher than that of
genes on any other chromosome (Short 1997a). This is
because any genetic defects cannot be `repaired' by
meiotic crossing over with a homologous chromosome.
Furthermore, the Ychromosome never enters female germ
cells, and germ-line mutations are known to be far more
common in the testis than the ovary (Short 1997a,b).
Considering the many millions of years of reproductive
isolation of the dromedary and the guanaco, it is perhaps
surprising that any male hybrids were produced at all.
Rama is living proof that the sex-determining genes on
the camel Y chromosome are still capable of inducing
testicular development in the hybrid. However, it seems
likely that Rama will prove to be sterile, both because
of the generalized meiotic failure observed in the
ovaries of the hybrids, and the expected di¡erences
between Y-linked spermatogenesis-determining genes in
the dromedary and the guanaco.
This study was kindly sponsored by H. H. Sheikh Mohammed
bin Rashid al Maktoum, Crown Prince of Dubai. We wish to
thank Professor Ulrich Wernery for his help with post-mortem
examinations, Bruce Abaloz for assistance with histology and
David Paul for the photomicrography. Dr K. Benirschke kindly
provided sections of the newborn guanaco ovary.
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656 J. A. Skidmore and others Hybrids between camels and guanacos
Proc. R. Soc. Lond. B (1999)
... However, interspecies mating and fertile hybrids are observed among some species. Skidmore et al. (1999) have reported hybrids of Old and New World camelids-C. dromedarius  L. guanicoe guanacos/llama and male camel. ...
... Milestone achievements in reproduction biotechniques in camelidsYearAchievements and remarks (references) 1960 First Camelid offspring from AI in Bactrian camel(Elliot 1961(Elliot ) 1998Production of hybrids of Old and New World camelids (Skidmore et al. 1999)2002Pregnancy established from transfer of vitrified-warmed Illama (Lama glama) embryos (Aller et al. 2002); successful transfer of vitrified-warmed embryos in Llama (Aller et al. 2002)2004First offspring after transfer of frozen-thawed embryos in C. dromedarius (Skidmore et al. 2004) 2005 Birth of C. dromedarius calves from transfer of cryopreserved embryos (Nowshari et al. 2005); pregnancy/live birth from transfer of vitrified warmed C. dromedarius camel (Skidmore et al. 2005) 2006 First calf from IVM, IVF, and in vitro cultured abattoir-derived dromedary camel oocytes (Khatir and Anouassi 2006) 2010 Birth of "Injaz," the first SCNT cloned C. dromedarius camel calf, using cumulus cells as donor nuclei (Wani et al. 2010) 2016 De novo gene assembly of a domestic dromedary of North African origin (Fitak et al. 2016) 2017 Developing interspecies cloned camel embryos using oocytes from C. bactreanus, and fibroblasts from C. bactreanus and L. glama; first birth of SCNT cloned C. bactreanus using dromedary camel as source of oocytes as well as surrogate female (Wani et al. 2017) 2018 Comprehensive studies on developmental competence of SCNT cloned embryos developed from various donor cells; cumulus cells found to be more suitable donor nuclei (Wani et al. 2018), evidences that cumulus cells of antral follicles are multipotent stem cell-like cells (Saadeldin et al. 2018) 2019 First description of near-chromosome assembly of the dromedary camel (Ruvinskiy et al. 2019), diversity analysis of C. dromedaries females in Morocco (Boujenane et al. 2019), induction of superovulation in C. dromedarius (Manjinatha et al. 2019) ...
Over the past three decades, similar to equine industry, various reproduction biotechniques, viz. artificial insemination, in vitro production of embryos, and nuclear transfer cloning, are developed for camelids. Inadequate understanding of reproduction physiology, incomplete genetic cataloguing of native genotypes, and lack of oocyte and proven embryo banks are the challenges in fully utilizing the reproduction potential of camels. This chapter presents an overview of advances and the bottlenecks of assisted reproduction technologies applied to camelids. Prospects of conservation of diversity of the species are discussed.
... identifying the actual parents for understanding divergence and reproductive incompatibilities (Edmands, 2002). The putative parents of the hybrid specimen, P. superciliaris and the N. meleagris, are estimated to have diverged ~65 MYA (Kumar et al., 2017 (Skidmore et al., 1999). The most diverged fish hybrid was produced in the laboratory and is between Polyodon spathula (American paddlefish) and Acipenser gueldenstaedtii (Russian sturgeon), estimated to have diverged ~150 MYA (Káldy et al., 2020). ...
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The most diverged avian hybrid that has been documented (Numida meleagris × Penelope superciliaris) was reported in 1957. This identification has yet to be confirmed, and like most contemporary studies of hybridization, the identification was based on phenotype, which can be misleading. In this study, we sequenced the specimen in question and performed analyses to validate the specimen's parentage. We extracted DNA from the specimen in a dedicated ancient DNA facility and performed whole‐genome short‐read sequencing. We used BLAST to find Galliformes sequences similar to the hybrid specimen reads. We found that the proportion of BLAST hits mapped overwhelmingly to two species, N. meleagris and Gallus gallus. Additionally, we constructed phylogenies using avian orthologs and parsed the species placed as sister to the hybrid. Again, the hybrid specimen was placed as a sister to N. meleagris and G. gallus. Despite not being a hybrid between N. meleagris and P. superciliaris, the hybrid still represents the most diverged avian hybrid confirmed with genetic data. In addition to correcting the “record” of the most diverged avian hybrid, these findings support recent assertions that morphological and behavioral‐based identifications of avian hybrids can be error‐prone. Consequently, this study serves as a cautionary tale to researchers of hybridization. In this article, Alfieri and colleagues revisit the identification of a historic avian hybrid, and using modern genetic techniques, correct the identification, while also correcting the record of the most diverged avian hybrid.
... In our previous study of cross-species painting in camelids [25] it was observed that the size of CDR 4 was greater than in other camelids, in that part of its long arm contained more GC rich heterochromatin than in related species. This is well illustrated in a camel:guanaco hybrid animal, which is heterozygous for this heteromorphic chromosome [25,26]. These observations on the variable size of alpaca homologues were confirmed recently when we sorted the alpaca chromosomes and found that the VPA homologue of CDR 4 was in a lower position at VPA peak D in the alpaca flow karyotype than in the dromedary flow karyotype (Figs. 2 and 4). ...
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Background The history of comparative chromosome mapping is briefly reviewed, with discussion about the problem that occurs in chromosome painting when size heteromorphisms between homologues cause contamination in chromosomes sorted by flow cytometry that are used in the preparation of chromosome-specific DNA probes. Main body As an example, we show in the alpaca ( Vicagna pacos ) that sequencing of contaminated chromosome sorts can reveal chromosome homologies from alignment with human and mouse genome reference sequences. The procedure identifies syntenic blocks of DNA separated in the human karyotype that are associated in the closely related alpaca and dromedary ( Camelus dromedarius ) karyotypes. This example provides proof of principal for the validity of the method for comparative chromosome mapping. Conclusion It is suggested that the approach presented here may have application in the construction of comparative chromosome maps between distantly related taxa, such as monotremes and mammals.
... The camel and llama possessed some anatomical and physiological similarities as a similar number of diploid chromosomes, and the left horn is larger than the right one [34][35][36]. Llama has a small size, cloven hoof, and dense wool layer until tolerating a low temperature, while the camel had one broad footpad and scaly hair coat [37]. ...
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Background The 3D computed tomography produces detailed images of the digit bones in addition to the angiograph render volume 3D of the CT shows the relation between the arteries, bones, and tissues of the digit. Therefore, the present study used those imaging techniques to provide a complete description of the digit bones and arteries’ origin, distribution, and course and their relations with surrounding structures in the Dromedary Camel. Which would serve as a guide for surgeons and students in distinguishing normal digit structures. The study used eight hind limbs of four adult camels of both sexes (two males and two females), aged 9–15 years (Mean ± SD, 11.80 ± 2.59 years). The samples were injected with latex with lead oxide were undergone 3D render volume CT (128-slice multi-detector CT scanning protocol) and angiography x-rays. Results The blood vessels and correlated structures such as bones, tendons, and ligaments were examined using 3D CT in all directions, which was easier to view than angiography and dissected specimens. The arterial supply to the camel’s hind foot was the A. digitalis plantaris communis III. The angiography render volume 3D of CT explained the blood supply of the bones and joints of digital regions and showed a good visualization of the many digit arteries. The metatarsals, the phalanges, and the sesamoid bones were visualized. A. plantaris medialis superficialis, A. digitalis plantaris communis III, A. digitalis plantaris communis II and IV, A. interdigitalis, rami articularis medialis and lateralis to the fetlock joint, ramus medialis and ramus lateralis of the A. digitalis plantaris communis III, A. digitalis plantaris propriae III et IV abaxialis, A. digitalis plantaris propriae III et IV axialis, Ramus phalangis axialis and abaxialis of the first phalanx, Ramus phalangis axialis and abaxialis of the second and third phalanges, and A. metatarsae plantaris III were visualized. The study discovered new blood vessel sources in dromedary camels, such as the ramus articularis to the fetlock and the ramus plantaris phalangis abaxialis proximalis and distalis of the first phalanx. Conclusions The digital circulation angiography investigates the circulatory pattern of the camel hind digit, which can assist clinicians in diagnosing digit region affections. 3D CT explained improved visualization of bones and arteries, including many small branches in relation to surrounding structures, in some views better than others.
... Since spermatozoa are separated from seminal plasma as well as selecting the robust spermatozoa (44), the method could be beneficial in extracting camelid spermatozoa from seminal plasma. Of the different selection techniques, colloid centrifugation looks to be quite promising, at least for llama spermatozoa (10,19), and is now used regularly when preparing dromedary camel semen for reproductive biotechnologies (45). Use of a low density gradient made from a colloid designed for human spermatozoa was also reported for preparing alpaca spermatozoa (5). ...
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Reproductive biotechnologies such as artificial insemination could be very useful for South American camelids, allowing widespread use of semen from breeding males with desirable genetics. However, artificial insemination is not widely employed in these species and is considered to have low overall efficiency. This is due in part to incomplete knowledge about the physiology of conception in these species, and also to challenges presented by semen collection and handling. Several recent reviews have centered on female camelid reproduction; therefore, in this review, the focus is on semen handling. Various semen collection methods are presented. Different methods of reducing seminal viscosity are compared, such as needling, enzyme treatment, and colloid centrifugation. Use of enzymes remains controversial because of widely differing results among research groups. Colloid centrifugation, particularly single layer centrifugation, has proved to be successful in facilitating development of sperm handling techniques in dromedary camels, and has also been used with llama semen. Therefore, protocols for colloid centrifugation of alpaca semen could be developed in the future.
... According to the author, the allantois is adhered to the entire chorionic surface, and the amnion is adhered to the allantois at the level of the pregnant horn. The left horn is always the largest and pregnant horn (Aba, 2014;Brown, 2000;Skidmore, Billah, Binns, Short, & Allen, 1999). ...
Macroscopic evaluation of the placenta is an essential postpartum examination in the alpaca and can be of special interest in case of abortion, premature‐ or stillbirth. Since there are not many reference values regarding macroscopic properties of normal alpaca placentas, a small descriptive study was conducted. Only placentae from normally foaling alpaca mares, giving birth to healthy crias, after a full‐term and uneventful gestation (± 350 days; range 335‐360 days) were taken into account (N = 11). Crias weighed (± SD) 7.7 ± 2.25 kg (range 5.5‐10 kg), while the mean weight of the full‐term placentas was 0.8 ± 0.19 kg, i.e. 10% of the bodyweight of the crias. The weight of the allantoamnion and chorion was 0.2 ± 0.07 kg and 0.5 ± 0.13 kg respectively. The umbilical cord length was 8.8 ± 2.84 cm and the length of the pregnant and non‐pregnant uterine horns were 69.4 ± 12.77 cm and 54.5 ± 6.81 cm respectively. The length of the corpus was 14.6 ± 4.68 cm and the distance from the umbilicus to the corpus was 18.5 ± 6.13 cm. The tissue volume of the allantoamnion was 0.14 ± 0.079 l and the chorionic volume was 0.37 ± 0.078 l. The surface area of the allantoamnion and the chorion was 87.6 ± 15.56 dm² and 72.3 ± 9.28 dm² respectively. All placentas had small calcifications either around the umbilical cord alone or around the umbilicus and blood vessels of the pregnant uterine horn. These measurements could be used to macroscopically evaluate alpaca placentas, although more research is needed to extend our knowledge of macroscopic evaluation of normal and abnormal placentas. This article is protected by copyright. All rights reserved.
... All four species of New World camelids are capable of interbreeding and producing fertile offspring without apparent reduced fecundity, as are the two species of Old World camels (reviewed in Skidmore at al., 2001). Despite geographic separation for at least the last 11 million years, hybridization between Old and New World camelids has also been documented through the use of artificial insemination and transfer of hybrid embryos (Skidmore et al.,1999(Skidmore et al., , 2001. Fecundity of Old x New World crosses, however, is very low. ...
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The four species of New World camelids and 2 species of Old World camelids derived from a common ancestor in North America. The reproductive characteristics, particularly those involving ovarian function and ovulation, are remarkably similar among the 6 living species of camelids, so much so that interspecies hybrids of nearly all possible combinations have been documented. Camelids are induced-ovulators, triggered by an ovulation-inducing factor in seminal plasma. The timing and mechanism of endocrine events leading to ovulation are discussed, as well as the discovery, identification and mode of action of the seminal factor responsible. The applied aspects of our present understanding are discussed with specific reference to controlled induction of ovulation, ovarian synchronization, and superovulation. Emphasis has been given to the literature on llamas and alpacas, with some reference to studies done in wild species of South American camelids and Old World camels.
The domesticated camelids of the world have had a significant impact on civilizations throughout recorded history. Populations of camels, referred to as Old World Camelids, are indigenous to Africa and Asia, while South American camelids, also called New World Camelids (NWCs), have evolved in the countries along the western mountains of South America. NWCs include alpacas, llamas, guanacos, and vicunas. Camelid evolution began in North America over 40 million years ago during the Eocene epoch. The cradle of llama domestication is the Andean puna (elevation 4000–4900 m), probably around Lake Titicaca, at approximately 5000–4000 BCE. Camels are an important part of the culture of the nomadic peoples of Asia and the Middle East, supplying food (meat and milk), fuel (the fecal pellets), fiber (clothing, ropes), leather, transportation (packing, riding), and racing.
Admixture, the genetic exchange between differentiated populations appears to be common in the history of species, but has not yet been comparatively studied across mammals. This limits the understanding of its mechanisms and potential role in mammalian evolution. The authors want to summarize the current knowledge on admixture in non‐human primates, and suggest that it is important to establish a comparative framework for this phenomenon in humans. Genetic observations in domesticated mammals and their wild counterparts are discussed, and a brief global overview on other clades is presented. Based on this, some of the consequences of gene flow, including incompatibilities and their genomic footprint, as well as adaptive introgression are discussed, and suggestions for a functional genomics approach are made. It is proposed that the field is moving beyond descriptive observations in single species, to a comprehensive analysis of admixture and its impact. Admixture is becoming an integral part of mammalian evolution. Admixture appears to be common in evolution, suggesting that it should be studied comparatively across mammals. Here, gene flow in non‐human primates and domesticated and other mammals is discussed. Consequences of admixture are adaptive introgression and genetic incompatibilities with their genomic footprints, which need to be understood using functional genomics approaches.
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This is a 133-page bibliography listing a wide variety of published works bearing on the topic of mammalian hybridization. More than 2,300 publications are listed.
Ten years ago a symposium on Cytotaxonomy 'was held in London (Proc. Linn. Soc. Lond. 169:110, 1958) in which a first attempt was made to bring together various disciplines to discuss advances of mammalian cytogenetics and to put them into proper context with the sciences of evolution and taxonomy. The introductory remarks by \V. B. Turrill to that symposium, essentially an admonishment to be tolerant of the short­ comings of our respective disciplines, would be a most appropriate begin­ ning to this conference as ,,'ell. However, the meeting held at Hanover was conceived more along the lines of remarks made by R. B. Seymour Se,,'ell in his presidential address to the same society: "It has been said that scientists in this search for truth are nowadays too much concerned with the accumulation of facts, and make too little use of their imagina­ tion in their attempts to explain such facts as they have accumulated. " (In "The continental drift theory and the distribution of the Copepoda," ibid. 166:149, 1956. ) \\Tith this as a background, two years ago we held the first of a series of loosely-structured conferences on reproductive failure in the relaxing atmosphere of this small New England college community. The manu­ scripts of that meeting have been published (Comparative Aspects of Re­ productive Failure, Springer-Verlag New York Inc. , 1967).
Recent findings suggest that many human fetuses have to adapt to a limited supply of nutrients and in doing so they permanently change their physiology and metabolism. These "programmed" changes may be the origins of a number of diseases in later life, including coronary heart disease and the related disorders stroke, diabetes, and hypertension. (C) Williams & Wilkins 1996. All Rights Reserved.
c1 Professor DJP Barker MD, PhD, FRCP, FRCOG, Director, MRC Environmental Epidemiology Unit, Southampton General Hospital, Southampton SO9 4XY, UK.
When in theF 1 offspring of a cross between two animal species or races one sex is absent, rare, or sterile, that sex is always the heterozygous sex.
The breeding season in the camel appears to be longer than was previously thought. The camel is an induced ovulator, and the estrous cycles are either ovulatory or non-ovulatory (follicular). The length of the estrous period depends on whether and when mating occurs. However, in both conditions, maximum estrogen concentration in the blood lasts for 2.9 ± 1.83 days. The concentration of LH in the peripheral blood plasma reaches its peak 2-4 h after mating or insemination, while ovulation occurs after 36-48 h. The developing CL can be detected by rectal palpation 10 days after service. Regression of the CL is rapid after sterile mating. Hence a CL similar to that of diestrus in other farm animals is not found in the camel. The ovulatory activity of the left ovaries (50.2-56.5%) is slightly higher than that of the right (43.5-49.8%), but left horn pregnancy is usual (98.2-100%). Multiple ovulations occur in 12.4-18.6% of camels but twin births are very rarely, if ever, observed. Pregnancy is characterized by the presence of a large and well developed CL which is maintained throughout pregnancy. Milk or blood progesterone can be a valuable tool for assessing early pregnancy in camels. Palpable swelling of the left horn is recognised 6-8 weeks after mating. Uterine involution is completed 40 ± 2.1 days after parturition. Suckling, lactation and nutrition are known to influence the interval to post-partum estrus. Low reproductive performance in camels is mainly ascribed to old age at first calving, long calving interval and limited breeding season. High abortion rate in some studies and the quite high calf mortality rate also contribute to low reproductive efficiency with long-term effects on herd dynamics.